Comparison of intra- and inter-host genetic diversity in rabies virus during experimental cross-species transmission.
The development of high-throughput genome sequencing enables accurate measurements of levels of sub-consensus intra-host virus genetic diversity and analysis of the role played by natural selection during cross-species transmission. We analysed the natural and experimental evolution of rabies virus...
Main Authors: | , , , , , , , , , |
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Format: | Article |
Language: | English |
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Public Library of Science (PLoS)
2019-06-01
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Series: | PLoS Pathogens |
Online Access: | https://doi.org/10.1371/journal.ppat.1007799 |
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author | Emilie M Bonnaud Cécile Troupin Laurent Dacheux Edward C Holmes Elodie Monchatre-Leroy Marion Tanguy Christiane Bouchier Florence Cliquet Jacques Barrat Hervé Bourhy |
author_facet | Emilie M Bonnaud Cécile Troupin Laurent Dacheux Edward C Holmes Elodie Monchatre-Leroy Marion Tanguy Christiane Bouchier Florence Cliquet Jacques Barrat Hervé Bourhy |
author_sort | Emilie M Bonnaud |
collection | DOAJ |
description | The development of high-throughput genome sequencing enables accurate measurements of levels of sub-consensus intra-host virus genetic diversity and analysis of the role played by natural selection during cross-species transmission. We analysed the natural and experimental evolution of rabies virus (RABV), an important example of a virus that is able to make multiple host jumps. In particular, we (i) analyzed RABV evolution during experimental host switching with the goal of identifying possible genetic markers of host adaptation, (ii) compared the mutational changes observed during passage with those observed in natura, and (iii) determined whether the colonization of new hosts or tissues requires adaptive evolution in the virus. To address these aims, animal infection models (dog and fox) and primary cell culture models (embryo brain cells of dog and fox) were developed and viral variation was studied in detail through deep genome sequencing. Our analysis revealed a strong unidirectional host evolutionary effect, as dog-adapted rabies virus was able to replicate in fox and fox cells relatively easily, while dogs or neuronal dog cells were not easily susceptible to fox adapted-RABV. This suggests that dog RABV may be able to adapt to some hosts more easily than other host variants, or that when RABV switched from dogs to red foxes it lost its ability to adapt easily to other species. Although no difference in patterns of mutation variation between different host organs was observed, mutations were common following both in vitro and in vivo passage. However, only a small number of these mutations also appeared in natura, suggesting that adaptation during successful cross-species virus transmission is a complex, multifactorial evolutionary process. |
first_indexed | 2024-12-16T09:13:43Z |
format | Article |
id | doaj.art-c47eca9c1a1e4683a08d38d84849f8ea |
institution | Directory Open Access Journal |
issn | 1553-7366 1553-7374 |
language | English |
last_indexed | 2024-12-16T09:13:43Z |
publishDate | 2019-06-01 |
publisher | Public Library of Science (PLoS) |
record_format | Article |
series | PLoS Pathogens |
spelling | doaj.art-c47eca9c1a1e4683a08d38d84849f8ea2022-12-21T22:36:57ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742019-06-01156e100779910.1371/journal.ppat.1007799Comparison of intra- and inter-host genetic diversity in rabies virus during experimental cross-species transmission.Emilie M BonnaudCécile TroupinLaurent DacheuxEdward C HolmesElodie Monchatre-LeroyMarion TanguyChristiane BouchierFlorence CliquetJacques BarratHervé BourhyThe development of high-throughput genome sequencing enables accurate measurements of levels of sub-consensus intra-host virus genetic diversity and analysis of the role played by natural selection during cross-species transmission. We analysed the natural and experimental evolution of rabies virus (RABV), an important example of a virus that is able to make multiple host jumps. In particular, we (i) analyzed RABV evolution during experimental host switching with the goal of identifying possible genetic markers of host adaptation, (ii) compared the mutational changes observed during passage with those observed in natura, and (iii) determined whether the colonization of new hosts or tissues requires adaptive evolution in the virus. To address these aims, animal infection models (dog and fox) and primary cell culture models (embryo brain cells of dog and fox) were developed and viral variation was studied in detail through deep genome sequencing. Our analysis revealed a strong unidirectional host evolutionary effect, as dog-adapted rabies virus was able to replicate in fox and fox cells relatively easily, while dogs or neuronal dog cells were not easily susceptible to fox adapted-RABV. This suggests that dog RABV may be able to adapt to some hosts more easily than other host variants, or that when RABV switched from dogs to red foxes it lost its ability to adapt easily to other species. Although no difference in patterns of mutation variation between different host organs was observed, mutations were common following both in vitro and in vivo passage. However, only a small number of these mutations also appeared in natura, suggesting that adaptation during successful cross-species virus transmission is a complex, multifactorial evolutionary process.https://doi.org/10.1371/journal.ppat.1007799 |
spellingShingle | Emilie M Bonnaud Cécile Troupin Laurent Dacheux Edward C Holmes Elodie Monchatre-Leroy Marion Tanguy Christiane Bouchier Florence Cliquet Jacques Barrat Hervé Bourhy Comparison of intra- and inter-host genetic diversity in rabies virus during experimental cross-species transmission. PLoS Pathogens |
title | Comparison of intra- and inter-host genetic diversity in rabies virus during experimental cross-species transmission. |
title_full | Comparison of intra- and inter-host genetic diversity in rabies virus during experimental cross-species transmission. |
title_fullStr | Comparison of intra- and inter-host genetic diversity in rabies virus during experimental cross-species transmission. |
title_full_unstemmed | Comparison of intra- and inter-host genetic diversity in rabies virus during experimental cross-species transmission. |
title_short | Comparison of intra- and inter-host genetic diversity in rabies virus during experimental cross-species transmission. |
title_sort | comparison of intra and inter host genetic diversity in rabies virus during experimental cross species transmission |
url | https://doi.org/10.1371/journal.ppat.1007799 |
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